Cited by 1,532Nerve injury and regenerationNeuroscience and Neuropharmacology ResearchAxon Guidance and Neuronal Signaling

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DEVELOPMENT OF THE VERTEBRATE NEUROMUSCULAR JUNCTION

Sanes, Joshua R., Lichtman, Jeff W.·1999·Annual Review of Neuroscience

DOI 10.1146/annurev.neuro.22.1.389

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Abstract

▪ Abstract We describe the formation, maturation, elimination, maintenance, and regeneration of vertebrate neuromuscular junctions (NMJs), the best studied of all synapses. The NMJ forms in a series of steps that involve the exchange of signals among its three cellular components—nerve terminal, muscle fiber, and Schwann cell. Although essentially any motor axon can form NMJs with any muscle fiber, an additional set of cues biases synapse formation in favor of appropriate partners. The NMJ is functional at birth but undergoes numerous alterations postnatally. One step in maturation is the elimination of excess inputs, a competitive process in which the muscle is an intermediary. Once elimination is complete, the NMJ is maintained stably in a dynamic equilibrium that can be perturbed to initiate remodeling. NMJs regenerate following damage to nerve or muscle, but this process differs in fundamental ways from embryonic synaptogenesis. Finally, we consider the extent to which the NMJ is a suitable model for development of neuron-neuron synapses.

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Depolarization-transcription signals in skeletal muscle use calcium flux through L channels, but bypass the sarcoplasmic reticulum
Huang, C., Flucher, B. E., Schmidt, M. M., Stroud, S. K., & Schmidt, J. (1994) · Neuron · doi:10.1016/0896-6273(94)90467-7 · Cited by 43
Retracted
The Molecular Biology of Axon Guidance
Tessier‐Lavigne, M., & Goodman, C. S. (1996) · Science · doi:10.1126/science.274.5290.1123 · Cited by 3,311
The synaptic vesicle cycle: a cascade of protein–protein interactions
Südhof, T. C. (1995) · Nature · doi:10.1038/375645a0 · Cited by 1,991
Molecular diversity of myofibrillar proteins: gene regulation and functional significance
Schiaffino, S., & Reggiani, C. (1996) · Physiological Reviews · doi:10.1152/physrev.1996.76.2.371 · Cited by 1,545
Nerve, Muscle and Synapse
Katz, B. (1966) · Medical Entomology and Zoology · Cited by 1,410
Multiple essential functions of neuregulin in development
Meyer, D., & Birchmeier, C. (1995) · Nature · doi:10.1038/378386a0 · Cited by 1,273
Molecular and cellular biology of cholinesterases
Massoulié, J., Pezzementi, L., Bon, S., Krejci, E., & Vallette, F.-M. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90040-y · Cited by 1,214
THE EPHRINS AND EPH RECEPTORS IN NEURAL DEVELOPMENT
Flanagan, J. G., & Vanderhaeghen, P. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.309 · Cited by 1,091
Molecular distinction between fetal and adult forms of muscle acetylcholine receptor
Mishina, M., Takai, T., Imoto, K., Noda, M., Takahashi, T., Numa, S., Methfessel, C., & Sakmann, B. J. (1986) · Nature · doi:10.1038/321406a0 · Cited by 1,000
Defective neuromuscular synaptogenesis in agrin-deficient mutant mice.
Gautam, M., Noakes, P., Moscoso, L. M., Rupp, F., Scheller, R., Merlie, J., & Sanes, J. (1996) · Cell · doi:10.1016/s0092-8674(00)81253-2 · Cited by 941
Self-citation

Show all 403 references

Research works printed but not linked: 10

Aframian D, 1988, Puerto Rico Health Sci. J., 7, 80
Bewick GS, 1996, J. Neurocytol., 25, 367
Brand-Saberi B, 1996, Int. J. Dev. Biol., 40, 411
Burgess RW, 1998, Neurosci. Abstr., 24, 1534
Ganju P, 1995, Oncogene, 11, 281
Laskowski MB, 1998, Neurosci. Abstr., 24, 791
Martin D, 1996, Am. J. Physiol., 271, R1422
Patton BL, 1995, Neurosci. Abstr., 20, 799
Serpinskaya AS, 1997, Neurosci. Abstr., 23, 33
Zhou H, 1998, Neurosci. Abstr., 24, 1534

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Swann, J. W., Al‐Noori, S., Jiang, M., & Lee, C. L. (2000) · Hippocampus · doi:10.1002/1098-1063(2000)10:5 · Cited by 268
A synaptic laminin–calcium channel interaction organizes active zones in motor nerve terminals
Nishimune, H., Sanes, J. R., & Carlson, S. S. (2004) · Nature · doi:10.1038/nature03112 · Cited by 276
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Zhang, W., & Benson, D. L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05169.2001 · Cited by 262
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Low, L. K., & Cheng, H.-J. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1883 · Cited by 258
Age-associated alterations of the neuromuscular junction
Jang, Y. C., & Remmen, H. V. (2010) · Experimental Gerontology · doi:10.1016/j.exger.2010.08.029 · Cited by 258
Fast and reversible trapping of surface glycine receptors by gephyrin
Meier, J. C., Vannier, C., Sergé, A., Triller, A., & Choquet, D. (2001) · Nature Neuroscience · doi:10.1038/85099 · Cited by 257
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Authors: Sanes, J. R., & Lichtman, J. W.
Affiliations: Washington University in St. Louis (US)
ORCID: Sanes, Joshua R.
Lichtman, Jeff W.
Venue: Annual Review of Neuroscience
Publisher: Annual Reviews
Published: 1999-03
Volume: 22
Issue: 1
Pages: 389-442
ISSN: 0147-006X (ISSN-L)
1545-4126
DOI: 10.1146/annurev.neuro.22.1.389
OpenAlex: W2134505400
Cited by: 1,532
References: 403
Citations by year: 2026: 22 · 2025: 36 · 2024: 47 · 2023: 35 · 2022: 35 · 2021: 47 · 2020: 60 · 2019: 44 · 2018: 48 · 2017: 55 · 2016: 49 · 2015: 27 · 2014: 57 · 2013: 39 · 2012: 57
FWCI: 8.58
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
Keywords: neuromuscular junction, synaptogenesis, synapse maturation, synaptic pruning, synapse maintenance, synaptic remodeling, neuromuscular junction regeneration, motor axons, muscle fibers, Schwann cells, vertebrate development
MeSH terms: Animals, Glycoproteins, Nerve Regeneration, Neuromuscular Junction, Synapses, Transcription, Genetic, Vertebrates, Signal Transduction, Presynaptic Terminals, Neuregulins

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DEVELOPMENT OF THE VERTEBRATE NEUROMUSCULAR JUNCTION

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